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As a youngster, Collins sang on radio stations in Windsor and Detroit. In 1940, at age 14, she and her family were introduced to bandleader/composer Raymond Scott in Chicago. Shortly thereafter, she became Scott's protégée. In early 1942, at age 15, she became a featured vocalist with Scott's orchestra, performing on radio and on tour. Scott groomed her for stardom, which included coaching her vocals (pitch, phrasing, and delivery) and mentoring her performance skills. In the late 1940s, she contributed vocals to the revived Raymond Scott Quintette, a sextet that released records on the bandleader's own Master label and served as house band on the radio program Herb Shriner Time. In 1949, after Scott was hired to conduct the orchestra on the popular CBS Radio program, Lucky Strike's Your Hit Parade, Collins was trained by Scott to lead his sextet on tour in his absence.

In 1950, Your Hit Parade moved to NBC television, with Scott retained as conductor. Shortly thereafter, at Scott's urging, Collins auditioned for a vocalist slot and was hired. She shot to nationwide fame as one of the show's featured vocalists, singing—and acting in costume—in sketches dramatizing popular songs of the day. After her absence from Your Hit Parade during the 1957–58 season (a new cast of singers replaced Collins and her fellow vocalists), Collins returned for the series' final season on CBS Television ending in April 1959.[2]

In 1955, her single "My Boy - Flat Top," reached #16 on the Billboard charts.[5] A follow-up single, "Baciare Baciare (Kissing Kissing)," peaked at #43. In 1956 her single "Seven Days" peaked at #17. She recorded other singles and albums in the 1950s, with little chart success. In 1958 for the Coral Records label she released Picnic: Dorothy Collins Sings Steve Allen, an album of compositions by the musician/TV host/comedian. Collins sang a collection of educational tunes on an album entitled Experiment Songs, one of six LPs in a set called Ballads for the Age of Science, composed and produced by Hy Zaret and Lou Singer around 1960.

In 1971, Collins made her Broadway debut in Stephen Sondheim's Follies, portraying Sally Durant Plummer,[7] a one-time Ziegfeld-style showgirl trapped in a disappointing marriage. Critic Martin Gottfried wrote of her performance: "Dorothy Collins, 'Hit Parade' jokes notwithstanding, has a voice of impressive versatility and range."[8] Her performance earned a Tony Award nomination as Best Actress in a Musical, but lost to co-star, fellow Canadian-born actress Alexis Smith.[9] When the production opened in Los Angeles in 1972, Collins reprised the role of Sally.[7]

Collins was married to Raymond Scott from 1952[1] until their divorce in 1965. They had two daughters, Deborah and Elizabeth. She married actor Ron Holgate in December 1966,[12] with whom she had a daughter, Melissa. They separated in 1977, and divorced in 1980.[13]